ADAM: A Disintegrin And Metalloproteinase; ADAM-8-/-: ADAM-8 deficient mice; ADAM-8+/+: ADAM-8 wild-type mice; sADAM-8: soluble form of ADAM-8
Abstract :
[en] Asthma is a complex disease linked to various pathophysiological events including the activity of proteinases. The multifunctional A Disintegrin And Metalloproteinases (ADAMs) displaying the ability to cleave membrane-bound mediators or cytokines appear to be key mediators in various inflammatory processes. In the present study, we have investigated ADAM-8 expression and production in a mouse model of allergen-induced airway inflammation. In allergen-exposed animals, increased expression of ADAM-8 was found in the lung parenchyma and in dendritic cells purified from the lungs. The potential role of ADAM-8 in the development of allergen-induced airway inflammation was further investigated by the use of an anti-ADAM-8 antibody and ADAM-8 knock-out animals. We observed a decrease in allergen-induced acute inflammation both in BALF and the peribronchial area in anti-ADAM-8 antibody-treated mice and in ADAM-8 deficient mice (ADAM-8-/-) after allergen exposure. ADAM-8 depletion led to a significant decrease of the CD11c+ lung dendritic cells. We also report lower levels of CCL11 and CCL22 production in antibody-treated mice and ADAM-8-/- mice that might be explained by decreased eosinophilic inflammation and lower numbers of dendritic cells, respectively. In conclusion, ADAM-8 appears to favour allergen-induced acute airway inflammation by promoting dendritic cell recruitment and CCL11 and CCL22 production.
Quesada Calvo, Florence ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Hacha, Jonathan ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Bekaert, Sandrine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Desmet, Christophe ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement
Bureau, Fabrice ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
ADAM-8, a metalloproteinase, drives acute allergen-induced airway inflammation
Publication date :
2011
Journal title :
European Journal of Immunology
ISSN :
0014-2980
eISSN :
1521-4141
Publisher :
VCH Verlagsgesellschaft, Weinheim, Germany
Volume :
41
Issue :
2
Pages :
380-91
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
FP7 - 201279 - MICROENVIMET - Understanding and fighting metastasis by modulating the tumour microenvironment through interference with the protease network.
Bousquet, J., Chanez, P., Lacoste, J. Y., Barneon, G., Ghavanian, N., Enander, I., Venge, P. et al., Eosinophilic inflammation in asthma. N. Engl. J. Med. 1990. 323: 1033-1039.
Bousquet, J., Chanez, P., Lacoste, J. Y., White, R., Vic, P., Godard, P. and Michel, F. B., Asthma: a disease remodeling the airways. Allergy 1992. 47: 3-11.
Kumar, R. K., Herbert, C. and Foster, P. S., The "classical" ovalbumin challenge model of asthma in mice. Curr. Drug Targets 2008. 9: 485-494.
Cataldo, D. D., Tournoy, K. G., Vermaelen, K., Munaut, C., Foidart, J. M., Louis, R., Noel, A. and Pauwels, R. A., Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation. Am. J. Pathol. 2002. 161: 491-498.
Gueders, M. M., Balbin, M., Rocks, N., Foidart, J. M., Gosset, P., Louis, R., Shapiro, S. et al., Matrix metalloproteinase-8 deficiency promotes granulocytic allergen-induced airway inflammation. J. Immunol. 2005. 175: 2589-2597.
Corry, D. B., Rishi, K., Kanellis, J., Kiss, A., Song Lz, L. Z., Xu, J., Feng, L. et al., Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency. Nat. Immunol. 2002. 3: 347-353.
Edwards, D. R., Handsley, M. M. and Pennington, C. J., The ADAM metalloproteinases. Mol. Aspects Med. 2008. 29: 258-289.
Seals, D. F. and Courtneidge, S. A., The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 2003. 17: 7-30.
Rocks, N., Paulissen, G., El Hour, M., Quesada, F., Crahay, C., Gueders, M., Foidart, J. M. et al., Emerging roles of ADAM and ADAMTS metalloproteinases in cancer. Biochimie 2008. 90: 369-379.
Primakoff, P. and Myles, D. G., The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet. 2000. 16: 83-87.
Van Eerdewegh, P., Little, R. D., Dupuis, J., Del Mastro, R. G., Falls, K., Simon, J., Torrey, D. et al., Association of the ADAM33 gene with asthma and bronchial hyperresponsiveness. Nature 2002. 418: 426-430.
Foley, S. C., Mogas, A. K., Olivenstein, R., Fiset, P. O., Chakir, J., Bourbeau, J., Ernst, P. et al., Increased expression of ADAM33 and ADAM8 with disease progression in asthma. J. Allergy Clin. Immunol. 2007. 119: 863-871.
Yoshida, S., Setoguchi, M., Higuchi, Y., Akizuki, S. and Yamamoto, S., Molecular cloning of cDNA encoding MS2 antigen, a novel cell surface antigen strongly expressed in murine monocytic lineage. Int. Immunol. 1990. 2: 585-591.
Yoshiyama, K., Higuchi, Y., Kataoka, M., Matsuura, K. and Yamamoto, S., CD156 (human ADAM8): expression, primary amino acid sequence, and gene location. Genomics 1997. 41: 56-62.
Gomez-Gaviro, M., Dominguez-Luis, M., Canchado, J., Calafat, J., Janssen, H., Lara-Pezzi, E., Fourie, A. et al., Expression and regulation of the metalloproteinase ADAM-8 during human neutrophil pathophysiological activation and its catalytic activity on L-selectin shedding. J. Immunol. 2007. 178: 8053-8063.
Kataoka, M., Yoshiyama, K., Matsuura, K., Hijiya, N., Higuchi, Y. and Yamamoto, S., Structure of the murine CD156 gene, characterization of its promoter, and chromosomal location. J. Biol. Chem. 1997. 272: 18209-18215.
Richens, J., Fairclough, L., Ghaemmaghami, A. M., Mahdavi, J., Shakib, F. and Sewell, H. F., The detection of ADAM8 protein on cells of the human immune system and the demonstration of its expression on peripheral blood B cells, dendritic cells and monocyte subsets. Immunobiology 2007. 212: 29-38.
Choi, S. J., Han, J. H. and Roodman, G. D., ADAM8: a novel osteoclast stimulating factor. J. Bone Miner. Res. 2001. 16: 814-822.
Schlomann, U., Rathke-Hartlieb, S., Yamamoto, S., Jockusch, H. and Bartsch, J. W., Tumor necrosis factor alpha induces a metalloprotease-disintegrin, ADAM8 (CD 156): implications for neuron-glia interactions during neurodegeneration. J. Neurosci. 2000. 20: 7964-7971.
Di Valentin, E., Crahay, C., Garbacki, N., Hennuy, B., Gueders, M., Noel, A., Foidart, J. M. et al., New asthma biomarkers: lessons from murine models of acute and chronic asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009. 296: L185-L197.
King, N. E., Zimmermann, N., Pope, S. M., Fulkerson, P. C., Nikolaidis, N. M., Mishra, A., Witte, D. P. and Rothenberg, M. E., Expression and regulation of a disintegrin and metalloproteinase (ADAM) 8 in experimental asthma. Am. J. Respir. Cell Mol. Biol. 2004. 31: 257-265.
Matsuno, O., Miyazaki, E., Nureki, S., Ueno, T., Kumamoto, T. and Higuchi, Y., Role of ADAM8 in experimental asthma. Immunol. Lett. 2006. 102: 67-73.
Schlomann, U., Wildeboer, D., Webster, A., Antropova, O., Zeuschner, D., Knight, C. G., Docherty, A. J. et al., The metalloprotease disintegrin ADAM8. Processing by autocatalysis is required for proteolytic activity and cell adhesion. J. Biol. Chem. 2002. 277: 48210-48219.
Amour, A., Knight, C. G., English, W. R., Webster, A., Slocombe, P. M., Knauper, V., Docherty, A. J. et al., The enzymatic activity of ADAM8 and ADAM9 is not regulated by TIMPs. FEBS Lett. 2002. 524: 154-158.
Naus, S., Reipschlager, S., Wildeboer, D., Lichtenthaler, S. F., Mitterreiter, S., Guan, Z., Moss, M. L. and Bartsch, J. W., Identification of candidate substrates for ectodomain shedding by the metalloprotease-disintegrin ADAM8. Biol. Chem. 2006. 387: 337-346.
Fourie, A. M., Coles, F., Moreno, V. and Karlsson, L., Catalytic activity of ADAM8, ADAM15, and MDC-L (ADAM28) on synthetic peptide substrates and in ectodomain cleavage of CD23. J. Biol. Chem. 2003. 278: 30469-30477.
Naus, S., Richter, M., Wildeboer, D., Moss, M., Schachner, M. and Bartsch, J. W., Ectodomain shedding of the neural recognition molecule CHL1 by the metalloprotease-disintegrin ADAM8 promotes neurite outgrowth and suppresses neuronal cell death. J. Biol. Chem. 2004. 279: 16083-16090.
Matsuno, O., Kumamoto, T. and Higuchi, Y., ADAM8 in allergy. Inflamm. Allergy Drug Targets 2008. 7: 108-112.
Paulissen, G., Rocks, N., Quesada-Calvo, F., Gosset, P., Foidart, J. M., Noel, A., Louis, R. and Cataldo, D. D., Expression of ADAMs and their inhibitors in sputum from patients with asthma. Mol. Med. 2006. 12: 171-179.
Tremblay, K., Lemire, M., Potvin, C., Tremblay, A., Hunninghake, G. M., Raby, B. A., Hudson, T. J. et al., Genes to diseases (G2D) computational method to identify asthma candidate genes. PLoS ONE 2008. 3: e2907.
Matsuno, O., Miyazaki, E., Nureki, S., Ueno, T., Ando, M., Ito, K., Kumamoto, T. and Higuchi, Y., Elevated soluble ADAM8 in bronchoalveolar lavage fluid in patients with eosinophilic pneumonia. Int. Arch. Allergy Immunol. 2007. 142: 285-290.
Kelly, K., Hutchinson, G., Nebenius-Oosthuizen, D., Smith, A. J., Bartsch, J. W., Horiuchi, K., Rittger, A. et al., Metalloprotease-disntegrin ADAM8: expression analysis and targeted deletion in mice. Dev. Dyn. 2005. 232: 221-231.
Bochner, B. S., Bickel, C. A., Taylor, M. L., MacGlashan, D. W., Jr., Gray, P. W., Raport, C. J. and Godiska, R., Macrophage-derived chemokine induces human eosinophil chemotaxis in a CC chemokine receptor 3- and CC chemokine receptor 4-independent manner. J. Allergy Clin. Immunol. 1999. 103: 527-532.
Ponath, P. D., Qin, S., Ringler, D. J., Clark-Lewis, I., Wang, J., Kassam, N., Smith, H. et al., Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 1996. 97: 604-612.
Gonzalo, J. A., Pan, Y., Lloyd, C. M., Jia, G. Q., Yu, G., Dussault, B., Powers, C. A. et al., Mouse monocyte-derived chemokine is involved in airway hyperreactivity and lung inflammation. J. Immunol. 1999. 163: 403-411.
Vulcano, M., Albanesi, C., Stoppacciaro, A., Bagnati, R., D'Amico, G., Struyf, S., Transidico, P. et al., Dendritic cells as a major source of macrophage-derived chemokine/CCL22 in vitro and in vivo. Eur. J. Immunol. 2001. 31: 812-822.
Lebre, M. C., Burwell, T., Vieira, P. L., Lora, J., Coyle, A. J., Kapsenberg, M. L., Clausen, B. E. and De Jong, E. C., Differential expression of inflammatory chemokines by Th1- and Th2-cell promoting dendritic cells: a role for different mature dendritic cell populations in attracting appropriate effector cells to peripheral sites of inflammation. Immunol. Cell Biol. 2005. 83: 525-535.
Chiba, Y., Onoda, S., Hattori, Y., Maitani, Y., Sakai, H. and Misawa, M., Upregulation of ADAM8 in the airways of mice with allergic bronchial asthma. Lung 2009. 187: 179-185.
Naus, S., Blanchet, M. R., Gossens, K., Zaph, C., Bartsch, J. W., McNagny, K. M. and Ziltener, H. J., The metalloprotease-disintegrin ADAM8 is essential for the development of experimental asthma. Am. J. Respir. Crit. Care Med. 181: 1318-1328.
Bedoret, D., Wallemacq, H., Marichal, T., Desmet, C., Quesada Calvo, F., Henry, E., Closset, R. et al., Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J. Clin. Invest. 2009. 119: 3723-3738.